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Journal of Thermal Biology

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Thermal biology of eastern box turtles in a longleaf pine system managedwith prescribed fire

John H. Roe⁎, Kristoffer H. Wild, Carlisha A. HallDepartment of Biology, University of North Carolina Pembroke, Pembroke, NC 28372, USA

A R T I C L E I N F O

Keywords:Habitat useTerrapene carolinaTemperatureThermal qualityThermoregulationReptile

A B S T R A C T

Fire can influence the microclimate of forest habitats by removing understory vegetation and surface debris.Temperature is often higher in recently burned forests owing to increased light penetration through the openunderstory. Because physiological processes are sensitive to temperature in ectotherms, we expected fire-maintained forests to improve the suitability of the thermal environment for turtles, and for turtles to seasonallyassociate with the most thermally-optimal habitats. Using a laboratory thermal gradient, we determined thethermal preference range (Tset) of eastern box turtles, Terrapene carolina, to be 27–31 °C. Physical models si-mulating the body temperatures experienced by turtles in the field revealed that surface environments in a fire-maintained longleaf pine forest were 3 °C warmer than adjacent unburned mixed hardwood/pine forests, but thefire-maintained forest was never of superior thermal quality owing to wider Te fluctuations above Tset andexposure to extreme and potentially lethal temperatures. Radiotracked turtles using fire-managed longleaf pineforests maintained shell temperatures (Ts) approximately 2 °C above those at a nearby unburned forest, but weobserved only moderate seasonal changes in habitat use which were inconsistent with thermoregulatory be-havior. We conclude that turtles were not responding strongly to the thermal heterogeneity generated by fire inour system, and that other aspects of the environment are likely more important in shaping habitat associations.

1. Introduction

Fire disturbance plays a critical role in the maintenance of structureand function in many habitats worldwide (Wright and Bailey, 1982;Nowacki and Abrams, 2008), with strong implications for the ecologyand evolution of biota (Keeley and Rundel, 2005; Beerling and Osborne,2006; Pausas and Keeley, 2009). Fire can directly kill, injure, or damagebiota by exposure to extreme temperatures, but among the most im-portant impacts of fire are indirect changes to the microclimate. Forinstance, while most prescribed fires do not remove overstory trees, theremoval of ground litter, debris, and vegetation can open the forestunderstory resulting in higher light levels and altered hydric and tem-perature conditions (Iverson and Hutchinson, 2002; Greenburg andWaldrop, 2008; Hossack et al., 2009). The magnitude and duration ofsuch effects and animal responses to them varies depending on habitat,fire frequency, intensity, and whether the fire was naturally ignited orintentionally set for management purposes (i.e., prescribed fire; Pastroet al., 2011; Elzer et al., 2013).

Environmental temperature directly influences the body tempera-ture (Tb) of ectotherms, which in turn strongly affects their physiology,behavior, and performance (Huey, 1982). In environments where

temperature varies spatially or temporally, ectothermic vertebratessuch as reptiles often behaviorally regulate Tb to maximize time at ornear temperatures where performance is optimized (Angilletta et al.,2002). The links between thermoregulatory behavior and temperature-sensitive performance should be strong owing to the influence of tem-perature on fitness-related activities and processes such as movement,energy and water balance, and reproduction (Huey and Slatkin, 1976;Huey and Bennett, 1987; Congdon, 1989). Canopy openings and un-derstory removal in fire-maintained habitats could thus offer moreopportunities to maintain Tb in the optimal performance range (Elzeret al., 2013). Indeed, many ectotherms respond positively to fire dis-turbance (Mushinsky, 1985; Ashton et al., 2008; Hossack et al., 2009;Matthews et al., 2010; Steen et al., 2013).

The eastern box turtle, Terrapene carolina, provides a useful modelto study the effects of post-fire habitat alteration on Tb and habitat use.T. carolina populations are typically found in a variety of forest types,often associating with canopy openings, habitat edges, and early suc-cessional or grassland habitat on a seasonal basis (Keister and Willey,2015). As Tb is strongly associated with environmental temperature inT. carolina (Adams et al., 1989), which in turn influences their perfor-mance and energy balance (Adams et al., 1989; Penick et al., 2002), the

http://dx.doi.org/10.1016/j.jtherbio.2017.09.005Received 2 August 2017; Received in revised form 16 September 2017; Accepted 18 September 2017

⁎ Corresponding author.E-mail addresses: john.roe@uncp.edu (J.H. Roe), kristofferwild@icloud.com (K.H. Wild), cah028@bravemail.uncp.edu (C.A. Hall).

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Available online 20 September 20170306-4565/ © 2017 Elsevier Ltd. All rights reserved.

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increased light penetration following fire could offer thermoregulatoryopportunities for this small-bodied terrestrial turtle. Alternatively, theincreased temperature under open canopies could at times expose themto lethal extremes, requiring movement out of openings and into moreshaded forest environments. For instance, in a study on turtle responsesto silvicultural management, T. carolina experienced considerablyhigher Tb in areas where the canopy was opened by timber harvesting,with associated modifications to their fine-scale movements and ac-tivity (Currylow et al., 2012). However, the limited mobility and smallhome range size of T. carolina may prohibit behavioral modificationsover broad spatial scales, though individuals and populations differ intheir vagility (Dodd, 2001; Currylow et al., 2012; Greenspan et al.,2015).

A large part of the range of T. carolina is in historically fire-pronehabitats, such as the southeastern Coastal Plain and Sandhills ecor-egions, which historically burned at a frequency of 1–3 and 4–6 years,respectively (Frost, 1998). Natural wildfires have been replaced in-creasingly by prescribed burning in an attempt to mimic this fire returninterval for silvicultural, hazard reduction, pest control, grazing, wild-life management, and biodiversity conservation purposes (Haines et al.,2001). However, we have little knowledge of the direct or indirect ef-fects of fire on T. carolina. Here, we investigate the potential for fire toimpact the thermal environments of T. carolina, and whether turtlesbehaviorally respond by seasonal changes in habitat use. We expect theopen canopy maintained by fire to increase both environmental tem-perature and turtle Tb, and that turtles will seasonally associate with themost thermally-optimal habitats.

2. Material and methods

2.1. Study site

The study was conducted at the Weymouth Woods Sandhills NaturePreserve (hereafter WEWO), a 202-ha state park in the sandhills phy-siographic region of south-central North Carolina. The habitat is amosaic of longleaf pine (Pinus palustris), loblolly pine (P. taeda), andhardwood trees in relatively equal proportion (40% longleaf, 33%hardwood, and 27% loblolly; J. Roe, unpubl. data). Longleaf occursprimarily in the xeric uplands, except where fire has been excluded orwhere loblolly were replanted in remnant forestry plantations.Hardwood forests, including mixed oak (Quercus spp.), hickory (Caryaspp.), red maple (Acer rubrum), sweetgum (Liquidambar styraciflua),American holly (Ilex opacum), sassafras (Sassafras albidum), and tulippoplar (Liriodendron tulipifera) trees are patchily distributed in uplandhabitats, but are primarily restricted to stream margins, bottomlandhabitats, and park units that have not been part of the prescribed fireprogram. In the upland areas where fire has been intentionally ex-cluded, a few large living remnant longleaf pine trees and stumps in-dicate that these habitats were once more populated with longleaf.Prescribed fire has been used in the park since 1974, with 76% of thearea being managed using controlled burns. Management units are12.9±7.8 ha (mean± standard deviation; 0.9–23.9 ha range) in size,with a target burn frequency of 3–5 years.

2.2. Temperature preference trials

Fourteen Terrapene carolina adults (11 male, 3 female, carapacelength 120.3–148.2 mm, mass 340–500 g) were captured from 21August to 16 September 2014 for temperature preference trials. Allturtles appeared healthy, were uninjured, and females were unlikely tobe gravid at this time of year (typical nesting season is from May–Julyat this location, J. Roe pers. obs.). Turtles were housed at the Universityof North Carolina at Pembroke for three to seven days before trials.Individuals were kept in separate rubber bins with constant access towater, but were not fed while in captivity.

Tb was measured along a thermal gradient constructed from

plywood (170 cm × 50 cm × 25 cm) with a bottom of aluminumflashing covered by sand 2 cm deep. A temperature gradient was cre-ated using an overhead ceramic heat lamp and heat pads (ReptithermU.T.H., Zoo Med Laboratories, Inc., San Luis Obispo, CA) placed underthe aluminum and maintained at constant temperatures by a Herpstatthermostat (Spyder Robotics LLC, Chana, IL). The heat lamp was placed30 cm over one end of the gradient, with a heat pad maintained at 38 °Capproximately 40 cm from the same end. Another heat pad, maintainedat 27 °C, was placed halfway down the gradient. The room was con-stantly maintained at 15 °C, creating a relatively cold end opposite theheat lamp. Overhead lights were set on natural light cycles of 12L:12D(photophase starting at 0700 h and scotophase at 1900 h).Temperatures were spot checked at the beginning and end of each trialwith an infra-red thermometer. In addition, five temperature dataloggers (Thermocron iButton, Dallas Semiconductor, Dallas, TX) wereplaced in the sand along the thermal gradient and recorded tempera-tures every 5 min.

Turtles were fitted with a hermetically sealed tip insulated ther-mocouple (Omega Engineering, Inc., Norwalk, CT) inserted 2 cm intothe cloaca. Temperature was monitored with an EasyLog data logger(Lascar Electronics, Erie, PA) that recorded temperature every 5 min.Turtles were placed individually in the gradient and remained un-disturbed for 24 h. The initial three hours of recordings were discardedbefore analysis to allow turtles to become acclimated to the gradient.We determined the preferred body temperature, or set-point range (Tset)for each turtle from the bounds of the central 50% (i.e., the 25th and75th quartiles) of selected Tb (Hertz et al., 1993). Given the highlyskewed sex ratios, males and females were grouped together in allanalyses. Turtles had no access to food or water during the temperaturepreference trials, and were released at their point of capture followingcompletion of trials.

2.3. Operative environmental temperatures

We estimated the operative environmental temperature (Te), the Tbavailable to a non-thermoregulating ectotherm (Bakken, 1992), usingphysical models placed in various habitats in the field. Models werewater filled Snapware® plastic bins painted in a flat black and tanmottled pattern of the approximate size, dimensions (135 cm × 85 cm× 58 cm), and color of adult T. carolina in our study system. Internaltemperatures were recorded every hour using iButtons sealed in a blackrubber coating (Plasti Dip International, Blaine, MN). Models werecalibrated alongside two fresh turtle carcasses with iButton dataloggersrecording internal Tb and external shell temperature (Ts). One modeland carcass pair was placed on the surface in the open for 24 h, whilethe other model and carcass pair was buried in the nearby litter. Day-time conditions were mostly sunny (0–50% cloud cover) during modelcalibrations.

From May to November 2013, models were placed in five randomlyselected locations each in a fire-maintained longleaf forest unit and anadjacent mixed hardwood/non-longleaf pine unburned forest unitwhere fire has been intentionally excluded at least since the park beganthe prescribed fire program in 1974. The most recent fire was in May2012 in the longleaf habitat. Locations were selected using the “createrandom points” tool in ArcMap 10.1 (Environmental Systems ResearchInstitute, Redlands, CA, USA). Each forest unit was of similar topo-graphy (2–15% slopes), elevation (364–416 m), and soils (combinationsof sand, loamy sand, sand clay loam, sandy loam profiles; USDA NaturalResources Conservation Service). Models were placed 50–500 m fromtheir counterparts in the adjacent forest units. At each location, onemodel was placed on the surface, while another was placed under thenearest cover object (leaf litter, logs, grasses, or shrubs) under which wecommonly observed T. carolina to seek refuge. Models were rotated tonew random locations each week over a period of several weeks duringa spring (8 May to 18 June 2013), summer (16 July to 27 Aug 2013),and fall (22 Oct to 12 Nov 2013) sampling period. The rotations

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resulted in 25 unique locations for each surface-refuge model pair ineach habitat type per season in spring and summer, and 15 unique lo-cations in fall. The thermal quality (de) of each habitat type (longleaf ormixed hardwood/non-longleaf pine), position (surface or refuge), andseason (spring, summer, fall) combination was calculated as the meanof absolute values of deviations of Te from Tset (Hertz et al., 1993). Forsurface models, we also calculated the percentage of Te above the lowerbound of Tset, (% ≥ Tset) as an index of the degree to which Tset couldbe maintained in a given habitat by behavioral adjustments (i.e.,movement between surface and refuge positions). This final index as-sumes that suitable refuge microhabitats (litter, shrubs, woody debris)that did not exceed Tset were available for retreat when Te exceeds Tseton the surface.

2.4. Free-ranging turtle temperatures and habitat use

We captured turtles opportunistically and equipped them withradiotransmitters (RI-2B, 10–15 g, Holohil Systems Ltd., Carp, ON,Canada) using 5 min epoxy gel (Devcon, Solon, OH) in the field. Wetracked 27 turtles (14 male and 13 female) from WEWO and recordedTs for a subset of individuals (5 male and 7 female). Hourly Ts wasrecorded using iButton temperature dataloggers coated in black PlastiDip and attached to the rear of the carapace. For comparison, we in-clude data from 23 turtles (12 male and 11 female; five of each sexequipped with iButtons) radiotracked at a site 24 km to the south on theborder of the Sandhills and Upper Coastal Plain physiographic regions,the Lumber River State Park (LRSP). This park is comprised of mixedpine (39% loblolly, 0.5% longleaf) and hardwood (60%) forests whereprescribed fire has not been employed at least since 2001 when the parktook over management of the property (J. Roe unpubl. data).

We located telemetered turtles once per week using a receiver (R-1000, Communication Specialists, Orange, CA) and a Yagi antenna. Ateach location, we assessed the relative composition of tree types in theimmediate surrounding area using a CRUZ-ALL angle gauge (ForestrySuppliers, Inc., Jackson, MS, USA). This method involved rotating 360°while holding the angle gauge at head height at a standard length (~64 cm) from the observer's eye, and counting the number of tree trunksthat completely filled (or more than filled) the 10-factor gauge opening.Trees were grouped into three categories which included 1) longleafpine, 2) other non-longleaf pine species, and 3) hardwood species. Thenumber of trees in each category was counted, and the relative pro-portion of each category was calculated and used as an index of forestmicrohabitat composition. We assessed canopy openness at a subset oflocations (n = 518), which were the first 23±1 locations for the first23 turtles we studied (ten from LRSP and 13 from WEWO), excludingany locations where the turtle was moving. Canopy openness was as-sessed with a spherical densiometer facing the four cardinal directionsand scores averaged for a single estimate at each location.

2.5. Data analyses

We performed statistical analyses with SPSS 23.0 (SPSS, 2015).Males and females were pooled in all analyses. Where appropriate, weexamined the assumptions of homogeneity of variances and normality;when data failed to meet assumptions, they were transformed to ap-proximate normal distributions or equal variances. Statistical sig-nificance was accepted at the α ≤ 0.05 level.

We used linear regression to examine the relationships between thetemperature of physical models, carcass temperature, and shell tem-perature. We used paired t-tests to examine the degree to which modelsand Ts underestimated or overestimated carcass temperature. We ex-amined variation in the estimates derived from physical models usinganalysis of variance (ANOVA) with mean Te, de, and % ≥ Tset as thedependent variables, and habitat type, season, and habitat × season asthe independent variables. In the above analyses, both Te and de werelog10-transformed, and % ≥ Tset was arcsine square root transformed.

Data from physical models was not separated based on variation inenvironmental conditions (e.g., cloud cover, precipitation, and wind)that could influence heating and cooling rates.

We used ANOVA to examine differences in mean monthly Ts be-tween sites (WEWO and LRSP) for each month separately. We alsocalculated mean canopy openness and mean proportion representationof each tree class (longleaf pine, non-longleaf pines, and hardwood) foreach turtle. We used regression analyses to assess the relationshipsbetween canopy openness (dependent variable) and the proportionalrepresentation of each tree habitat class (independent variables). Bothcanopy openness and proportion representation values were arcsinesquare root transformed prior to analyses.

To examine seasonal variation in forest microhabitat use, we usedrepeated measures ANOVAs with month as the repeated variable andmean proportion of non-longleaf pine and hardwood trees as the de-pendent variables. We used Friedman tests to examine monthly varia-tion in use of longleaf pine, with month as the repeated variable andmean proportion of longleaf pine as the dependent variable. All pro-portional values were arcsine square root transformed. We restrictedour analysis of seasonal use of forest microhabitats to the active season,between May–October.

3. Results

3.1. Temperature preference

We obtained 3182 measurements of Tb from turtles in the thermalgradient. Tb ranged from 17.5 to 34.5 °C, with a mean (± SE) of28.8±0.6 °C. The 25% and 75% quartiles (Tset) averaged across in-dividuals was 27.0–31.0 °C (Fig. 1). Available temperatures along thegradient measured by dataloggers under the sand ranged from 18.5 to37.0 °C, while surface temperature directly under the heat lamp was ashigh as 45 °C.

3.2. Operative environmental temperatures

Temperature of physical models was correlated with Tb of turtlecarcasses (R2 = 0.963, F1,158 = 4115.2, P<0.001), but temperaturesof physical models deviated by as much as 6 °C above and 3 °C belowTb. Because models slightly underestimated Tb by 0.41±0.11 °C(paired t= 3.85, P<0.001), we adjusted temperatures of models usingthe equation:

= −body temperature 1.0215(model temperature) 0.1033

We recorded 19,600, 18,270, and 2012 measures of Te in the spring,summer, and fall seasons respectively. For surface positions, Te, de, and% ≥ Tset varied by habitat, season, and the interaction of these twovariables (Table 1). Surface Te ranged from 0 to 62 °C across habitatsand seasons and was highest in summer, intermediate in spring, andlowest in fall (Table 2, Fig. 2). Surface Te was approximately 3 °C higherin burned longleaf forests than in adjacent unburned mixed hardwood/

Fig. 1. Body temperatures (Tb) of eastern box turtles (Terrapene carolina) on a laboratorythermal gradient.

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non-longleaf pine forests in both spring and summer, but did not differbetween habitats in fall (Table 2). Surface de was lowest (i.e., of higherthermal quality) in summer, intermediate in spring, and highest in fallin all habitats (Table 2). Surface de was lower in unburned mixedhardwood/non-longleaf pine forests than adjacent burned longleafforests in the summer, but did not differ between habitats in spring orfall (Table 2). The amount of time Te was within or above Tset (% ≥Tset) was 17–20% higher in burned longleaf forests than in unburnedmixed hardwood/non-longleaf pine forests in spring and summer, butdifferences between habitats were minimal in fall (Table 2).

For refuge positions, Te and de varied by habitat, season, and theirinteraction, though the effect of habitat was only marginally significantfor Te (Table 1). Refuge Te ranged from 1 to 37 °C across habitats andseasons and was higher in burned longleaf forests than unburned mixedhardwood/non-longleaf pine forests in spring and summer, but did notdiffer between habitats in fall (Table 2, Fig. 3). Refuge de was lowest(i.e., of higher thermal quality) in summer, intermediate in spring, andhighest in fall in both habitats, and lower in burned longleaf foreststhan unburned mixed hardwood/non-longleaf pine forests in all seasons(Table 2).

In spring, hourly average Te remained above the minimum Tsetthreshold (27 °C) from 1100 to 1900 h on the surface in burned longleafhabitat, but neither refuge longleaf nor mixed hardwood/non-longleafpine (surface or refuge) habitats reached the minimum Tset threshold(Fig. 4). In summer, hourly average Te in burned longleaf habitatsreached the minimum Tset threshold from 1000 to 2000 h on the sur-face, and from 1300 to 2000 h in refuge habitats (Fig. 4). Summer

hourly average Te in unburned mixed hardwood/non-longleaf pinehabitats reached the minimum Tset threshold from 1300 to 1900 h onthe surface, but never reached Tset in refuge habitats (Fig. 4). Fallhourly average Te did not reach Tset in either habitat (Fig. 4).

3.3. Free-ranging turtle temperatures

Ts was correlated with Tb of carcasses (R2 = 0.912, F1,92 = 948.3,P<0.001), with Ts overestimating Tb by 0.70± 0.34 °C (paired t =2.06, P = 0.04). However, some measures of Ts deviated by as much as

Table 1Summary results of ANOVA for the effects of habitat type (longleaf forest or mixedhardwood and pine forest), season (spring, summer, or fall), and their interaction onoperative temperature (Te), thermal quality (de), and percentage of Te within or above Tset(% ≥ Tset) in surface and refuge positions.

Position Effect Metric num df den df F p

Surface Habitat Te 1 24 57.6 < 0.001de 1 24 30.2 < 0.001% ≥ Tset 1 24 99.4 < 0.001

Season Te 2 24 2364.1 < 0.001de 2 24 2010.4 < 0.001% ≥ Tset 2 24 376.3 < 0.001

Habitat × season Te 2 24 36.7 < 0.001de 2 24 21.6 < 0.001% ≥ Tset 2 24 11.4 < 0.001

Refuge Habitat Te 1 21 4.0 0.059de 1 21 10.3 0.004

Season Te 2 21 643.3 < 0.001de 2 21 266.3 < 0.001

Habitat × season Te 2 21 5.2 0.014de 2 21 4.9 0.018

Table 2Summary of seasonal habitat variation in operative environmental temperatures (Te), thermal quality (de), and percentage of time Te was within or above Tset (% ≥ Tset). The burnedforest was predominately longleaf pine, while the unburned forest was a mixture of hardwood and non-longleaf pine species.

Position Season Habitat Te °C (se) de (se) % ≥ Tset (se) Te °C range

Surface Spring Burned 24.7 (0.2) 5.3 (0.1) 31.4 (1.3) 7–62Unburned 21.8 (0.1) 5.4 (0.1) 11.0 (1.5) 8–37

Summer Burned 27.4 (0.2) 4.0 (0.1) 41.1 (1.7) 14–55Unburned 24.5 (0.1) 3.0 (0.1) 24.3 (1.9) 11–47

Fall Burned 13.0 (0.1) 14.0 (0.0) 1.2 (0.3) 0–32Unburned 13.4 (0.3) 13.5 (0.3) 0.2 (0.2) 1–31

Refuge Spring Burned 21.5 (0.2) 5.6 (0.2) – 10–37Unburned 20.3 (0.2) 6.7 (0.2) – 10–27

Summer Burned 25.2 (0.5) 2.4 (0.3) – 15–35Unburned 23.6 (0.2) 3.4 (0.2) – 16–32

Fall Burned 12.9 (0.2) 14.3 (0.2) – 4–25Unburned 13.4 (0.5) 13.7 (0.4) – 1–22

Fig. 2. Frequency distribution of seasonal operative environmental temperatures forsurface habitats in fire-maintained longleaf pine forests and unburned mixed hardwood/non-longleaf pine forests. Note that the grey color represents areas where the two habi-tats’ distributions overlap. The preferred body temperature, or set-point range (Tset) foreastern box turtles (Terrapene carolina) is 27–31 °C.

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15 °C above and 3 °C below Tb when on the surface.From 1 May–31 October, we obtained 28,896 and 29,640 measures

of Ts at WEWO and LRSP, respectively. Ts ranged from 1.5 to 43.5 °C atWEWO and from 1.0 to 42.0 °C at LRSP. Monthly mean Ts was0.4–1.8 °C higher at WEWO than LRSP (Fig. 5), but differed sig-nificantly only during August (F1,13 = 12.40, P = 0.004) and October(F1,13 = 8.08, P = 0.014). However, comparisons between sites formost other months approached significance (May: F1,14 = 3.95, P =0.067, June: F1,15 = 3.87, P = 0.068, July: F1,17 = 4.09, P = 0.059,August: F1,13 = 1.86, P = 0.196). The most pronounced differences inTs between sites occurred during the day between 1100–1700 h, whileovernight Ts was similar (Fig. 6).

3.4. Habitat use

Turtles used habitats with predominantly hardwood trees in allmonths at both sites, but the relative amounts of each tree class in thenearby habitat varied moderately over the course of the active season(Fig. 7). Turtles at WEWO used forests with increasing percentages ofnon-longleaf pine from May–October (F5,130 = 2.4, P = 0.042), whileusing forests with a decreasing percentage of hardwoods over the sametime period (F5,130 = 6.1, P<0.001; Fig. 7). At LRSP, turtles also usedforests with increasing percentage of non-longleaf pine from May–Oc-tober (F5,110 = 2.7, P = 0.046), but the percentage of hardwood treesin used forests did not vary over this time period (F5,130 = 1.8, P =0.147; Fig. 7). There was no seasonality of use for longleaf habitat ateither site (P>0.334; Fig. 7).

Variation in canopy openness depended on tree types in the im-mediate surrounding area. Canopy openness increased logarithmicallywith increasing percent longleaf (F1,11 = 25.4, R2 = 0.70, P<0.001),but decreased linearly with increasing percent hardwood trees (F1,9 =85.6, R2 = 0.91, P<0.001; Fig. 8). Canopy openness was not corre-lated with percent non-longleaf pine species (F1,9 = 1.6, P = 0.233).

4. Discussion

The use of prescribed fire in forest habitat management affects thethermal characteristics of the environment, and thus has the potentialto indirectly influence the physiology and behavior of ectothermicvertebrates such as turtles. Our results indicate that the burned longleafhabitat experienced considerably higher temperatures than the ad-jacent unburned mixed hardwood/non-longleaf pine forest, but surface

Fig. 3. Frequency distribution of seasonal operative environmental temperatures for re-fuge habitats in fire-maintained longleaf pine forests and unburned mixed hardwood/non-longleaf pine forests. Note that the grey color represents areas where the two habi-tats’ distributions overlap. The preferred body temperature, or set-point range (Tset) foreastern box turtles (Terrapene carolina) is 27–31 °C.

Fig. 4. Seasonal mean hourly operative environmental temperatures for surface and re-fuge models in fire-maintained longleaf pine forests and unburned mixed hardwood/non-longleaf pine forests. The preferred body temperature, or set-point range (Tset) for easternbox turtles (Terrapene carolina) is 27–31 °C.

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environments in the fire-managed longleaf forest were not of superiorthermal quality in any part of the active season. The longleaf forest alsohad a more variable thermal environment, where surface-active turtleswould be regularly exposed to temperatures above their thermal pre-ference range and sometimes exceeding lethal limits. Turtles using fire-managed longleaf forests experienced seasonally higher Ts, but despitethe potential thermal costs and benefits associated with the differenthabitats and seasons, there was little evidence to suggest habitat usebehaviors were linked to variation in the habitats’ thermal

characteristics.This is the first quantification of Tset for any subspecies of T. car-

olina. Our estimates of Tset (27.0–31.0 °C) and mean preferred Tb(28.8 °C) are higher than the preferred Tb reported for T. carolinaelsewhere (20–25 °C; Erskine and Hutchison, 1981; do Amaral et al.,2002a, 2002b). Compared more broadly to other species, our estimatesof preferred Tb are within the upper range reported for turtles fromtemperate regions; 20.7–22.4 °C for Sternotherus odoratus (Graham andHutchison, 1979); 21.1–24.9 °C for Clemmys guttata (Graham andHutchison, 1979); 22.0–27.0 °C for Glyptemys insculpta (Dubois et al.,2008); 22.0–27.2 °C for Chrysemys picta (Graham and Hutchison, 1979;Edwards and Blouin-Demers, 2007); 24.6–29.1 °C for Trachemys scripta(Gatten, 1974); 28.1 °C for Chelydra serpentina (Schuett and Gatten,1980); 28.3–29.8 °C for Terrapere ornata (Gatten, 1974), and28.7–32.5 °C for Graptemys geographica (Bulté and Blouin-Demers,2010). Temperature preferences in turtles can vary among populationsover latitudinal gradients, including in Terrapene spp. (Ellner andKarasov, 1993), and can even differ among individuals within a po-pulation exposed to different local thermal environments (Curtin,1998). Our study populations were from lower latitude and elevation(and thus a warmer climate) compared to most other species for whichpreferred Tb has been assessed, and the higher preferred Tb in our studyis consistent with observations of ectotherms from warmer climates(Ellner and Karasov, 1993). Turtles may also vary in thermal preferencedue to nutritional status (Gatten, 1974), infection (Monagas and Gatten,1983; do Amaral et al., 2002b), and perhaps other intrinsic factors. Oursample was limited to apparently healthy and postabsorptive adultturtles in the late active season when potentially confounding variationdue to reproductive status would also be minimized. Our estimates ofpreferred Tb were within the range of temperatures for optimized per-formance in turtles for feeding (29–30 °C, Gatten, 1974; 26–29 °C,Parmenter, 1980; 30 °C, Dubois et al., 2008) and locomotion (24–32 °C,

Fig. 5. Monthly shell temperatures (mean± SE) for field-active eastern box turtles(Terrapene carolina) at a site managed using prescribed fire (WEWO) compared to turtlesat an unburned site (LRSP).

Fig. 6. Hourly mean shell temperatures for field-active eastern box turtles (Terrapenecarolina) at a site managed using prescribed fire (WEWO) compared to turtles at an un-burned site (LRSP) during May, July, and September.

Fig. 7. Seasonal forest habitat use for eastern box turtles (Terrapene carolina) at A) a sitemanaged using prescribed fire (WEWO) compared to B) turtles at an unburned site(LRSP).

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Adams et al., 1989), further justifying our use of Tset estimates in as-sessing the suitability of the thermal environment for various importantprocesses in T. carolina.

The long-term use of prescribed fire in the longleaf pine system waslikely a strong contributor to the altered thermal environments avail-able to turtles at our site, resulting in part through changes in vegeta-tive structure. Fire reduces vegetative and ground cover, and opens thecanopy allowing more direct solar radiation to the forest floor(Mushinsky, 1992; Greenberg and Waldrop, 2008; Matthews et al.,2010), resulting in increased temperature for several years after fire(Hossack et al., 2009). Indeed, in areas where prescribed fire has beenregularly employed at our study site, where longleaf pines predominate,canopy openness was higher than in predominantly hardwood foresthabitats that are not managed with fire. That the higher mean surfaceTe in fire-maintained longleaf habitats was closer to Tset at first suggeststhis would be the most thermally-optimal habitat for T. carolina, yet thishabitat was never of superior thermal quality, likely due to its wider Tefluctuations. Minimum Te was similar among habitats, but surface Teexceeded Tset for 20–25% of recordings in burned longleaf forests inspring and summer compared to just 1–3% in unburned mixed hard-wood/non-longleaf pine habitats. Moreover, surface Te in fire-main-tained longleaf forests exceeded temperatures presumed to be lethal, or

the critical thermal maximum (CTmax), in turtles. While we did notmeasure CTmax in our study population, based on measures from otherstudies, we presume it unlikely that T. carolina would tolerate extendedexposure to temperatures above 40 °C (Sturbaum, 1981; Plummer et al.,2003; Lagarde et al., 2012). Consistent with this explanation, the onlytime when thermal quality differed between surface environments wasduring the hot summer period, when the unburned mixed hardwood/non-longleaf pine forest was of higher thermal quality due to the coolertemperatures. During this period, the more open fire-maintained long-leaf forest exceeded CTmax 7% of the time.

It is important to recognize that comparisons of thermal quality onlyreflect the relative availability of thermally favorable environmentswithout taking into consideration thermoregulatory behaviors. Manyreptiles maximize thermal benefits by shuttling among microhabitats oraltering position in thermally heterogeneous environments to remainwithin or closer to Tset for more extended periods (Christian andWeavers, 1996; Edwards and Blouin-Demers, 2007; Dubois et al., 2009;Besson and Cree, 2010). Assuming turtles in our study were behavio-rally thermoregulating, fire-maintained longleaf forest could offer moreopportunities to maintain Tb closer to or within Tset. For instance,surface Te exceeded the lower bound of Tset for 17% and 20% more ofthe time than in unburned mixed hardwood/non-longleaf pine forestsin summer and spring seasons, respectively, while refuge environmentsalways offered Te below the upper bound of Tset in both forest types atthese times. To exploit these opportunities in the fire-maintainedlongleaf habitat, suitable thermal refuge microsites would need to bereadily available, and turtles would need to move between surface andnearby refuge environments. We were not able to assess how carefullyturtles thermoregulated in the different habitats because we did notmeasure Tb in field-active animals. Instead, we measured Ts as an ap-proximation of Tb, as these two measures can be tightly linked in small-bodied turtles (Grayson and Dorcas, 2004). However, the degree towhich Ts accurately reflects Tb may differ among species due to shapeand size variation and their effects on heating and cooling rates (Polo-Cavia et al., 2009; Bulté and Blouin-Demers, 2010). While our measuresof Ts were correlated with Tb, the magnitude of deviations was at timeshigh, so we were cautious in using Ts as an accurate proxy of Tb for allscenarios in field-active turtles. Nevertheless, the higher Ts of turtles atthe fire-maintained site (WEWO) suggest they would have also ex-perienced relatively higher Tb than turtles at a nearby site where fire isnot used in management (LRSP). However, Ts differences between siteswere only moderate (< 2 °C), and whether this difference was a resultof habitat alterations from fire, or whether this resulted in measurablydifferent vital rates or performance measures is not yet known. We arecurrently monitoring growth rates, body condition, survivorship, andother endpoints that could elucidate any temperature effects with fit-ness consequences.

Turtles often respond to thermally heterogeneous environments bybehavioral thermoregulation, including habitat selection to maximizeheat gain (Dubois et al., 2009; Picard et al., 2011), alterations to ac-tivity timing and use of refuges in times of temperature extremes(Nieuwolt, 1996; Lagarde et al., 2012), and seasonal migration betweenareas differing in temperature (Swingland and Lessells, 1979). Giventhe variation in thermal characteristics of habitats at the fire-main-tained site, we expected to observe strong links between seasonal ha-bitat use and thermoregulatory behavior in T. carolina. As the fire-maintained and unburned forests occur in close proximity to one an-other at WEWO, turtles could hypothetically move between the dif-ferent habitats to maximize thermal benefits (maintain Tb closer to Tset)or minimize costs (avoid overheating) on a temporal basis. Indeed,individual turtles did regularly move between burned and unburnedhabitats and among different forest types. However, while we did ob-serve some seasonality in habitat use, the magnitude of changes wasonly moderate, and the directions of change were not consistent withbehavioral thermoregulation. For instance, use of the unburned, pre-dominantly hardwood forests should have peaked in summer when this

Fig. 8. Relationships between canopy openness and relative forest composition of hard-wood, longleaf pine, and non-longleaf pine trees at a site managed using prescribed fire.

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habitat offered superior thermal quality, but associations with suchenvironments decreased moderately (minus 14% from May to October)throughout the active season at WEWO and did not vary seasonally atLRSP. Likewise, if turtles were behaving in ways to minimize risks ofexposure to temperature extremes, use of the fire-maintained longleafforests should have decreased in summer, but we observed no season-ality in use of this habitat. We did observe moderately increased use offorests with more non-longleaf pine species at both sites over the activeseason (plus 6–8% from May to October), but because canopy opennessdid not vary according to this tree class, it is unlikely that this shift inhabitat use was driven by thermoregulation.

Habitat use is shaped by multiple requirements in including hy-dration, feeding, reproduction, and predator avoidance. While all ofthese processes are dependent on temperature in ectotherms (Huey,1982; Angilletta et al., 2002), perhaps the relatively low variation inthermal characteristics among habitats and overall benign thermalenvironment of our system minimizes the influence of temperature inhabitat use “decisions”. Ectotherms must invest more effort into ther-moregulation in extreme climates with low thermal quality, such as athigher latitudes and elevations (Blouin-Demers and Nadeau, 2005); as aresult, we typically see stronger thermoregulatory behaviors, such ashabitat selection and activity timing, in thermally challenging en-vironments (Blouin-Demers and Weatherhead, 2001; Edwards andBlouin-Demers, 2007; Besson and Cree, 2010). In our study, the largestdifference in thermal quality (de) between habitats in any season (forcomparable positions) was 1.1, and all habitats were of relatively highthermal quality during most of the active season compared to measuresfrom terrestrial habitats in colder climates (Blouin-Demers andWeatherhead, 2001; Blouin-Demers and Nadeau, 2005; Row andBlouin-Demers, 2006). T. carolina may thus be able to more easilymaintain Tb close to Tset in both fire-maintained and unburned forestswithout employing potentially costly thermoregulatory behaviors.

In the only other study of T. carolina in a longleaf system, turtlesselected predominantly hardwood and mixed pine-hardwood forestsand used predominantly pine forests (including longleaf) less often thanexpected based upon availability (Greenspan et al., 2015), which isconsistent with high use of hardwood forests in all seasons at our sites.However, longleaf pines accounted for approximately 21% of the treesin the microhabitats used by turtles at the fire-maintained site (WEWO),while accounting for less than 1% of forest composition at turtle loca-tions at the unburned site (LRSP). It should be noted that we did notassess habitat selection here, as this would require comparing habitatuse with availability. Our approach was simply to examine whetherseasonal shifts in the forest composition of the habitats used by turtlescould be linked to temporal variation in habitat thermal characteristics.As there were no major temporal or spatial changes in the availability ofoverstory trees in our study systems, an assessment of changes in ha-bitat use alone should be informative for detecting seasonal shifts inforest habitat associations. Further studies could assess whether asso-ciations with (or selection of) other aspects of the habitat structure(e.g., cover objects, water availability, understory vegetation structure)vary seasonally, or whether turtles respond to thermal heterogeneity atbroader spatial scales (i.e., macrohabitat or landscape scale distribu-tion). It would also be instructive to determine if turtles in the fire-maintained longleaf forest exhibit different seasonal shifts in surfaceactivity timing to avoid periods of extreme mid-day heat (Te> Tset from1200 to 1800), as has been observed in other terrestrial turtles inthermally challenging habitats (Meek, 1988; Plummer, 2003). Becauseno turtles died from overheating nor showed any signs of heat stress(other than some that were burned by fire), we suspect that they ex-hibited some degree of thermoregulatory behavior, but our samplingdesign of tracking turtles only once per week was insufficient to detectsuch fine-scale temporal variation in activity.

Our results suggest that T. carolina does not exhibit a strong beha-vioral response to the thermal heterogeneity created by prescribed firein our system at the spatial and temporal scales we examined. However,

we caution that our observations are from only on a single site wherefire disturbance has long been a natural part of the system and whereprescribed fire has been used in management for the last several dec-ades. Turtle responses to other fire regimes, habitats, or in other parts oftheir broad geographic range may be different than observed here. Ourstudy design was also limited in its ability to disentangle the manyenvironmental factors other than temperature that can influence ha-bitat use in turtles. Moreover, habitat associations and other behaviorscould be affected by the direct risks imposed by fire, as T. carolina cansuffer injury and mortality from burns (Babbitt and Babbit, 1951; Plattet al., 2010), as well as decreased body condition following fire (Howeyand Roosenburg, 2013). Fire could also indirectly affect habitat usebehavior by altering understory vegetation structure, hydric conditions,or food availability (Rossell et al., 2006; Platt et al., 2009; Greenspanet al., 2015). It is clear that as fire becomes a more popular tool forhabitat management, much more research is required to understand theresponses of T. carolina and other terrestrial ectotherms to both wildand prescribed fires.

Acknowledgements

We would like to thank C. Gause, J. Rowlett, J. Smink, C. Wilson, L.Baxley, G. Hoffmann, Z. Lunn, and C. Haywood for assistance withfieldwork. Research was conducted under protocol Roe-2011 issued bythe UNC Pembroke Institutional Animal Care and Use Committee andlicense SC00506 from the North Carolina Wildlife ResourcesCommission. This work was supported by the Lucille Stickel Fund,North Carolina Herpetological Society, Pembroke UndergraduateResearch Center, UNCP Teaching and Learning Center, UNCP BiologyDepartment, and the UNC Pembroke RISE program under the NationalInstitutes of General Medical Sciences Grant #5R25GM077634.

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